The rubber foot illusion
© Crea et al. 2015
Received: 20 February 2015
Accepted: 28 August 2015
Published: 4 September 2015
Lower-limb amputation causes the individual a huge functional impairment due to the lack of adequate sensory perception from the missing limb. The development of an augmenting sensory feedback device able to restore some of the missing information from the amputated limb may improve embodiment, control and acceptability of the prosthesis.
In this work we transferred the Rubber Hand Illusion paradigm to the lower limb. We investigated the possibility of promoting body ownership of a fake foot, in a series of experiments fashioned after the RHI using matched or mismatched (vibrotactile) stimulation. The results, collected from 19 healthy subjects, demonstrated that it is possible to elicit the perception of possessing a rubber foot when modality-matched stimulations are provided synchronously on the biological foot and to the corresponding rubber foot areas. Results also proved that it is possible to enhance the illusion even with modality-mismatched stimulation, even though illusion was lower than in case of modality-matched stimulation.
We demonstrated the possibility of promoting a Rubber Foot Illusion with both matched and mismatched stimulation.
The Rubber Hand Illusion (RHI) is a perceptual illusion causing the feeling of ownership of a realistic rubber hand when placed in full view and synchronously stimulated with the person’s own hand, which is hidden from view . The illusion happens as a result of the interaction and coherence of vision, touch and proprioception [2, 3] and it typically induces a shift of the perceived location of the participant’s hand towards the rubber hand (proprioceptive drift) and a strong skin conductance response (SCR) to a threat stimulus on the rubber hand. This illusion does not occur when the stimulations are not synchronous [1–3].
In recent years the paradigm of the RHI was investigated on different body parts, e.g. the tongue , the arm  or the entire body  and translated from basic neuroscience studies to different application scenarios, like virtual reality  or upper-limb prostheses [7–10]. Indeed Ehrsson and colleagues demonstrated that the RHI can be elicited even when the natural hand is missing, namely in upper-limb amputees when stimulated on referred phantom fingers on the stump . This finding suggested engineers to develop hand prostheses with tactile sensory feedback capable of promoting the embodiment of the prosthesis itself [7, 8]. In our previous studies we suggested and proofed the possibility of inducing the RHI using mismatched stimulation (i.e. sensory substitution) on healthy subjects  and transradial amputees . In particular we used miniaturized vibrotactile stimulators, that are small enough to be embedded in a prosthetic socket, conversely to current state-of-the-art haptic stimulators, too bulky .
Lower-limb amputation, similarly to upper-limb loss, causes the individual a huge functional impairment due to the lack of adequate sensory perception from the missing limb. While ambulation is generally a well-learned activity, which requires little or no cognitive effort by healthy adults , ambulating with an above-knee prosthesis is a cognitively demanding task, because the normal proprioceptive afferent flow is lost, and amputees find it difficult to control their prostheses, especially in unstructured environment, i.e. uneven terrain. The use of vision combined to a sensory feedback stimulation provided in a natural and intuitive fashion, (e.g. by exploiting the phantom limb sensation, as suggested by Murray  and Ehrsson and collegues ) could improve the controllability of the prosthesis, as tactile information from the prosthesis would match and enrich the information from the vision. At the same time, an intuitive proprioceptive feedback could also be an important asset in itself; in fact if the prosthesis could induce a feeling of ownership it is predictable that the ratio of unsatisfied patients will reduce .
In this work we transferred the RHI paradigm to the lower limb. The first goal of the study, similarly to the work recently published by Lenggenhager and collegues , was to investigate the possibility of promoting body ownership of a fake foot, in series of experiment fashioned after the RHI, using matched stimulation. The second goal of the study was to investigate the possibility to enhance the feeling of possessing a rubber foot when applying mismatched (vibrotactile) stimulation, which can be potentially integrated in a sensory feedback system for lower-limb prosthesis. The results, collected from 19 healthy subjects, demonstrated indeed the possibility of promoting a Rubber Foot Illusion (RFI) with both matched and mismatched stimulation.
Materials and methods
Questionnaire. Statements from 1 to 3 are illusion statements. Statements from 4 to 9 are suggestion statements. Statements 10 and 11 are respectively used to quantify the vividness and prevalence of the illusion
It seemed like I was feeling the stimulation in the point where the rubber foot was being touched
It seemed like the stimulation I was feeling was caused by the touch of the paintbrush on the rubber foot
I felt like the rubber foot was mine
I felt like my (real) foot was moving towards left (towards the rubber foot)
It seemed like I had more than one right foot and leg
It seemed like the stimulation I was feeling became from some places between my foot and the rubber foot
I felt like my (real) foot like was becoming rubbery
It seemed like the rubber foot was moving towards right (towards my real foot)
The rubber foot started to look like my (real) foot, in terms of shape, skin tone, o other characteristics
Using a score from 0 to 10, quantify the vividness (how much your illusion of a rubber foot was realistic)
Using a score from 0 to 100 %, quantify how long you had the illusion that the rubber foot was yours
The Kolgomorov-Smirnov test was used to verify whether the measurements were normally distributed. Then, two-way repeated-measures ANOVA (factors: timing and modality) was performed singularly for each measurement (i.e. questionnaires, drifts or SCR) in order to assess significant differences in the stimulation conditions. Similarly the results were pairwise compared using two-tailed paired t-test [15, 16], with Tukey-Kramer correction. Statistical significance was set to 0.05.
Results from the two-way repeated measures ANOVA showed a statistically significant interaction effect between the timing and modality on the vividness of the illusion (F(1,17)=7.37,p=.0147) (Fig.2 (b)). Significant main effects of timing (F(1,17)=70.62,p<.0001) and modality were found (F(1,17)=25.42,p=.0001). Post-hoc pairwise analysis revealed that, in both congruent and incongruent conditions, vividness scored significantly higher when stimulations were synchronous than in case they were asynchronous (t-test with Tukey-Kramer adjustment, CS vs CA p<.0001, IS vs IA p=.0009). Significantly higher vividness was also found in the CS compared to the IS (t-test with Tukey-Kramer adjustment, p<.0001) while no significant difference was found between CA and IA cases (t-test, p=.1182).
Two-way repeated-measures ANOVA applied on the prevalence scores (Fig.2 (c)) revealed again a significant interaction effect between timing and modality factors (F(1,17)=11.02,p=.0041), and two main effects for the timing (F(1,17)=91.68,p<.0001) and the modality (F(1,17)=22.31,p=.0002). Post-hoc analysis found that prevalence scored higher in synchronous conditions than in asynchronous ones (CS vs CA p<.0001; IS vs IA p=.0004). The effect of modality was also significant for prevalence scores (F(1,17)=22.31,p=.0002), and pairwise comparison resulted in higher prevalence in synchronous congruent condition than in synchronous incongruent one (CS vs IS p<.0001; CA vs IA p=.3346).1
Regarding the SCR measurements, the two-way ANOVA showed a significant main effect for the timing of the stimulations (F(1,18)=6.75,p=.0181), no significant main effect of the stimulation modality (F(1,18)=4.02,p=.0603) and no significant interaction effect (F(1,18)=3.5,p=.0777) (Fig.3 (b)). Pairwise comparison of different timing conditions revealed higher SCR in CS condition than in CA (p=.0054), while no difference was found between IS and IA (p=.6132). Since modality did not result in a main effect, pairwise comparison was not assessed.
Discussion and conclusions
The body schema is usually defined as a continuously updated sensorimotor map of the body that informs the brain about what parts belongs to the body and where those parts are located . The trick of the RHI is a direct consequence of multisensory integration, which basically misleads the brain as to the status of ownership of a fake hand, provoking its inclusion in the body schema. The largest part of neurophysiological studies has explored the body schema using stimulation to and near the hands. Hands may be considered special in that they are used for almost any kind of action we perform, but it seems that processing principles revealed for the hands may not generalize to other body parts . Indeed, combining multisensory information has different implications in case the stimuli come from different parts of the body’s surface. For example tactile information takes different amounts of time to be processed by the brain depending on the distance between the stimulated surface and the brain and some studies showed how the integration of visual and tactile stimulation of the foot can lead to bad perception of simultaneity of the stimuli . Our results provide evidence that it is possible to elicit the perception of possessing a rubber foot when modality-matched stimulations are provided synchronously on the biological foot and to the equivalent rubber foot areas. Indeed, all the three independent measurements of embodiment, classically employed in similar experiments on the RHI [9, 15, 21], gave closely matched results supporting this main outcome, thus confirming that even though visual and tactile stimulations applied on the foot undergo different processing mechanisms, the multisensory integration can still effectively compound the illusion and the brain integrates the fake foot in the body schema. Second to that, we investigated the RFI approach for application in the development of sensory feedback systems for lower-limb prostheses in order to provide the individual with information from the foot sole [22, 23]. Results proved that it is possible to enhance the illusion even with modality-mismatched stimulations, even though illusion was lower than in case of modality-matched stimulation. Notably asynchronous stimulation, which is used as a standard control test, in both modality congruent and incongruent cases did not induce the illusion, as reported also in previous studies [1, 3, 7–9, 13, 15]. These results open important perspectives in the field of lower-limb prosthetics; indeed, vibrotactile elements can be easily integrated into the socket of lower-limb prostheses in order to stimulate the referred phantom foot areas and induce the RFI on a daily basis. This feature could improve the controllability of the prosthesis  and enhance the satisfaction of the amputee in using the prosthesis even more .
Future studies will be devoted at investigating whether the proposed mismatched-stimulation paradigm can promote the embodiment of the prosthesis in the body schema of lower-limb amputees.
1 Eighteen of nineteen participants replied to vividness and prevalence questions.
The authors would like to thank Eng. M. Moisé for helping with artwork in (Fig.1). This work was partly supported by EU within the CYBERLEGs Project (Grant num. 287894) and the WAY Project (Grant num. 288551), and by Fondazione Pisa within the IUVO Project (prog. 154/11).
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License(http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
- Botvinick M, Cohen J. Rubber hands’ feel’touch that eyes see. Nature. 1998; 391(6669):756–6.View ArticlePubMedGoogle Scholar
- Ehrsson HH, Holmes NP, Passingham RE. Touching a rubber hand: feeling of body ownership is associated with activity in multisensory brain areas. J Neurosci. 2005; 25(45):10564–10573.PubMed CentralView ArticlePubMedGoogle Scholar
- Shimada S, Fukuda K, Hiraki K. Rubber hand illusion under delayed visual feedback. PLoS ONE. 2009; 4(7):6185.View ArticleGoogle Scholar
- Michel C, Velasco C, Salgado-Montejo A, Spence C. The butcher’s tongue illusion. Perception. 2014; 43:818–24.View ArticlePubMedGoogle Scholar
- Slater M, Perez-Marcos D, Ehrsson HH, Sanchez-Vives MV. Towards a digital body: the virtual arm illusion. Front Hum Neurosci. 2008;2:6. doi:10.3389/neuro.09.006.2008
- Van Der Hoort B, Guterstam A, Ehrsson HH. Being barbie: the size of one’s own body determines the perceived size of the world. PLoS ONE. 2011; 6(5):20195.View ArticleGoogle Scholar
- Ehrsson HH, Rosén B, Stockselius A, Ragnö C, Köhler P, Lundborg G. Upper-limb amputees can be induced to experience a rubber hand as their own. Brain. 2008; 131(12):3443–452.PubMed CentralView ArticlePubMedGoogle Scholar
- Marasco PD, Kim K, Colgate JE, Peshkin MA, Kuiken TA. Robotic touch shifts perception of embodiment to prosthesis on targeted reinnervation amputees. Brain. 2011; 134:747–58.PubMed CentralView ArticlePubMedGoogle Scholar
- D’Alonzo M, Cipriani C. Vibrotactile sensory substitution elicits feeling of ownership of an alien hand. PLoS ONE. 2012; 7(11):50756.View ArticleGoogle Scholar
- D’Alonzo M, Clemente F, Cipriani C. Vibrotactile stimulation promotes embodiment of an alien hand in amputees with phantom sensations. Neural Syst Rehabil Eng IEEE Trans. 2014; 23(3):450–7.View ArticleGoogle Scholar
- Abernethy B, Hanna A, Plooy A. The attentional demands of preferred and non-preferred gait patterns. Gait and Posture. 2002; 15:256–65.View ArticlePubMedGoogle Scholar
- Murray CD. Embodiment and prosthetics. Psychoprosthetics. London: Springer; 2008, pp. 119–129.Google Scholar
- Lenggenhager B, Hilti L, Brugger P. Disturbed body integrity and the “rubber foot illusion”. Neuropsychology. 2014; 29(2):205–11.View ArticlePubMedGoogle Scholar
- Cipriani C, D’Alonzo M, Carrozza MC. A miniature vibrotactile sensory substitution device for multifingered hand prosthetics. Biomed Eng IEEE Trans. 2012; 59(2):400–8.View ArticleGoogle Scholar
- Tsakiris M, Carpenter L, James D, Fotopoulou A. Hands only illusion: multisensory integration elicits sense of ownership for body parts but not for non-corporeal objects. Exp Brain Res. 2010; 204(3):343–52.View ArticlePubMedGoogle Scholar
- Howell D. Statistical methods for psychology. Cengage Learning. 2012. https://books.google.it/books?hl=it&lr=&id=CRYKAAAAQBAJ&oi=fnd&pg=PR5&dq=Statistical+methods+for+psychology&ots=au7JL5A_rU&sig=yTyZArv-ipiGqq4tJ46X9NRaacg#v=onepage&q=Statistical%20methods%20for%20psychology&f=false
- Tsakiris M, Haggard P. The rubber hand illusion revisited: visuotactile integration and self-attribution. J Exp Psychol Hum Percept Perform. 2005; 31(1):80.View ArticlePubMedGoogle Scholar
- De Vignemont F. Embodiment, ownership and disownership. Conscious Cogn. 2011; 20(1):82–93.View ArticlePubMedGoogle Scholar
- Ionta S, Fourkas AD, Fiorio M, Aglioti SM. The influence of hands posture on mental rotation of hands and feet. Exp Brain Res. 2007; 183(1):1–7.View ArticlePubMedGoogle Scholar
- Harrar V, Harris LR. Simultaneity constancy: detecting events with touch and vision. Exp Brain Res. 2005; 166(3-4):465–73.View ArticlePubMedGoogle Scholar
- Ehrsson HH, Spence C, Passingham RE. That’s my hand! activity in premotor cortex reflects feeling of ownership of a limb. Science. 2004; 305(5685):875–7.View ArticlePubMedGoogle Scholar
- Crea S, Vitiello N, De Rossi SMM, Lenzi T, Donati M, Cipriani C, et al. Development of an experimental set-up for providing lower-limb amputees with an augmenting feedback. Converging Clin Eng Res Neurorehabil. 2013; 1:321–325. http://link.springer.com/chapter/10.1007/978-3-642-34546-3_51 View ArticleGoogle Scholar
- Crea S, Cipriani C, Donati M, Carrozza MC, Vitiello N. Providing time-discrete gait information by wearable feedback apparatus for lower-limb amputees: usability and functional validation. Neural Syst Rehabil Eng, IEEE Trans. 2014:1–8. doi:10.1109/TNSRE.2014.2365548
- Kuiken TA, Marasco PD, Lock BA, Harden RN, Dewald JP. Redirection of cutaneous sensation from the hand to the chest skin of human amputees with targeted reinnervation. Proc. Nat Acad Sci USA. 2007; 104(50):20061–0066.PubMed CentralView ArticlePubMedGoogle Scholar